The genus Willisornis is endemic to the Amazon Basin, inhabiting upland terra firme forest, with two species and seven subspecies currently recognized. Despite numerous systematic studies, a taxonomically-dense sampled phylogeny for Willisornis is still lacking, which, combined with evidence of paraphyly and gene flow between its recognized species, underscores the uncertainty concerning species limits and evolutionary history of the genus. Here we present phylogenies and population genetic analyses, including all currently recognized Willisornis taxa, relating them to patterns of plumage variation, and reconstructing the spatiotemporal context of diversification in the genus. Our analyses have uncovered 13 independent genetic lineages in the genus, and the monophyly of all currently named taxa, which also showed robust plumage diagnoses. However, deeply coalesced genetic lineages were also found within most Willisornis taxa, for which no consistent variation in plumage was found. The diversification of the genus Willisornis is related to hydrographic and climate change cycles across Amazonia since the Plio-Pleistocene, with most genetic lineages originating in the past one million years. Based on our findings, we recommend the recognition of a total of six species in Willisornis (one of which polytypic) based on the congruency between deeply coalesced lineages and consistent plumage diagnoses.